Higher-order sensorimotor circuit of the brain's global network supports human consciousness.


Journal

NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515

Informations de publication

Date de publication:
01 05 2021
Historique:
received: 16 10 2020
revised: 29 12 2020
accepted: 08 02 2021
pubmed: 15 2 2021
medline: 16 10 2021
entrez: 14 2 2021
Statut: ppublish

Résumé

Consciousness is a mental characteristic of the human mind, whose exact neural features remain unclear. We aimed to identify the critical nodes within the brain's global functional network that support consciousness. To that end, we collected a large fMRI resting state dataset with subjects in at least one of the following three consciousness states: preserved (including the healthy awake state, and patients with a brain injury history (BI) that is fully conscious), reduced (including the N1-sleep state, and minimally conscious state), and lost (including the N3-sleep state, anesthesia, and unresponsive wakefulness state). We also included a unique dataset of subjects in rapid eye movement sleep state (REM-sleep) to test for the presence of consciousness with minimum movements and sensory input. To identify critical nodes, i.e., hubs, within the brain's global functional network, we used a graph-theoretical measure of degree centrality conjoined with ROI-based functional connectivity. Using these methods, we identified various higher-order sensory and motor regions including the supplementary motor area, bilateral supramarginal gyrus (part of inferior parietal lobule), supragenual/dorsal anterior cingulate cortex, and left middle temporal gyrus, that could be important hubs whose degree centrality was significantly reduced when consciousness was reduced or absent. Additionally, we identified a sensorimotor circuit, in which the functional connectivity among these regions was significantly correlated with levels of consciousness across the different groups, and remained present in the REM-sleep group. Taken together, we demonstrated that regions forming a higher-order sensorimotor integration circuit are involved in supporting consciousness within the brain's global functional network. That offers novel and more mechanism-guided treatment targets for disorders of consciousness.

Identifiants

pubmed: 33582277
pii: S1053-8119(21)00127-0
doi: 10.1016/j.neuroimage.2021.117850
pmc: PMC9583596
mid: NIHMS1840961
pii:
doi:

Substances chimiques

Anesthetics, Intravenous 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

117850

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM103894
Pays : United States
Organisme : CIHR
Pays : Canada

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest None declared.

Références

Cereb Cortex. 2019 Feb 1;29(2):648-656
pubmed: 29300881
Front Neurol. 2018 Nov 30;9:1024
pubmed: 30555407
Front Psychol. 2015 Jun 25;6:868
pubmed: 26161076
PLoS Comput Biol. 2013;9(10):e1003271
pubmed: 24146606
Arch Phys Med Rehabil. 2004 Dec;85(12):2020-9
pubmed: 15605342
Nat Rev Neurosci. 2012 Apr 13;13(5):336-49
pubmed: 22498897
Trends Cogn Sci. 2005 Dec;9(12):556-9
pubmed: 16271507
Nat Commun. 2019 Oct 10;10(1):4616
pubmed: 31601811
Anesthesiology. 1998 Jan;88(1):18-24
pubmed: 9447851
Neuron. 2011 Apr 28;70(2):200-27
pubmed: 21521609
Nat Neurosci. 2001 Jul;4(7):752-8
pubmed: 11426233
Front Psychol. 2013 May 13;4:256
pubmed: 23717291
Neuroimage. 2013 Apr 15;70:327-39
pubmed: 23313420
J Neurosci. 2007 Feb 28;27(9):2349-56
pubmed: 17329432
Cereb Cortex. 2015 Oct;25(10):3723-42
pubmed: 25331602
Neurology. 2007 Mar 20;68(12):895-9
pubmed: 17372124
Nat Rev Neurosci. 2016 Jul;17(7):450-61
pubmed: 27225071
Lancet. 2014 Aug 9;384(9942):514-22
pubmed: 24746174
Hum Brain Mapp. 2018 May;39(5):2035-2046
pubmed: 29377435
Ann Neurol. 2015 Oct;78(4):594-605
pubmed: 26290126
Neuroimage. 2018 May 15;172:642-653
pubmed: 29421324
PLoS Comput Biol. 2015 Apr 14;11(4):e1004225
pubmed: 25874700
J Neurosci. 2017 Oct 4;37(40):9603-9613
pubmed: 28978697
Anesthesiology. 2017 Mar;126(3):419-430
pubmed: 28092321
Front Neurosci. 2019 Feb 06;13:46
pubmed: 30787863
Brain. 2020 Apr 1;143(4):1177-1189
pubmed: 32101603
Elife. 2015 Nov 09;4:
pubmed: 26551562
Hum Brain Mapp. 2010 Dec;31(12):1993-2002
pubmed: 20336686
Front Hum Neurosci. 2013 Dec 26;7:910
pubmed: 24421764
Trends Cogn Sci. 2016 Dec;20(12):871-882
pubmed: 27765517
Brain. 2018 Nov 1;141(11):3179-3192
pubmed: 30285102
Anesth Analg. 2012 Mar;114(3):533-46
pubmed: 22253267
Hum Brain Mapp. 2014 Nov;35(11):5368-78
pubmed: 24867379
Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4489-94
pubmed: 19255447
Psychol Bull. 2020 Mar;146(3):218-244
pubmed: 32027149
Neuroimage. 2014 Nov 15;102 Pt 2:894-903
pubmed: 25067818
Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11376-81
pubmed: 19549821
Nat Neurosci. 2003 Feb;6(2):119-26
pubmed: 12555104
Nat Neurosci. 2017 Jun;20(6):872-878
pubmed: 28394322
Neurology. 2012 Jan 17;78(3):175-81
pubmed: 22218274
Neuron. 2015 Oct 7;88(1):145-66
pubmed: 26447578
Brain. 2010 Jan;133(Pt 1):161-71
pubmed: 20034928
N Engl J Med. 2010 Feb 18;362(7):579-89
pubmed: 20130250
Behav Brain Sci. 2001 Oct;24(5):939-73; discussion 973-1031
pubmed: 12239892
Proc Natl Acad Sci U S A. 2017 Sep 5;114(36):9713-9718
pubmed: 28827337
Nat Rev Neurosci. 2016 May;17(5):307-21
pubmed: 27094080
Sci Adv. 2019 Feb 06;5(2):eaat7603
pubmed: 30775433
Neuroimage. 2012 Feb 1;59(3):2142-54
pubmed: 22019881
Trends Cogn Sci. 2013 Dec;17(12):683-96
pubmed: 24231140
Neuroimage. 2016 Jan 1;124(Pt A):693-703
pubmed: 26343319
Anesthesiology. 2020 Jun;132(6):1392-1406
pubmed: 32205548
J Neurophysiol. 2011 Sep;106(3):1125-65
pubmed: 21653723
Science. 2006 Sep 8;313(5792):1402
pubmed: 16959998
Sleep. 2019 Mar 1;42(3):
pubmed: 30476346
JAMA Neurol. 2015 Dec;72(12):1413-5
pubmed: 26502348

Auteurs

Pengmin Qin (P)

Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education; School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China; Pazhou Lab, Guangzhou 510335, China. Electronic address: qin.pengmin@m.scnu.edu.cn.

Xuehai Wu (X)

Pazhou Lab, Guangzhou 510335, China; Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai Key laboratory of Brain Function Restoration and Neural Regeneration, Neurosurgical Institute of Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, China.

Changwei Wu (C)

Research Center for Brain and Consciousness, Taipei Medical University, Taipei, Taiwan; Graduate Institute of Humanities in Medicine, Taipei Medical University, Taipei, Taiwan; Shuang-Ho Hospital, Taipei Medical University, New Taipei, Taiwan.

Hang Wu (H)

Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education; School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China.

Jun Zhang (J)

Department of Anesthesiology, Fudan University Shanghai Cancer center, Shanghai, China.

Zirui Huang (Z)

Department of Anesthesiology and Center for Consciousness Science, University of Michigan, Ann Arbor, MI, USA.

Xuchu Weng (X)

Institute for Brain Research and Rehabilitation, South China Normal University, Guangzhou, Guangdong, China.

Di Zang (D)

Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai Key laboratory of Brain Function Restoration and Neural Regeneration, Neurosurgical Institute of Fudan University, Shanghai, China; State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, China.

Zengxin Qi (Z)

Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China.

Weijun Tang (W)

Radiology Department, Shanghai Huashan Hospital, Fudan University, Shanghai, China.

Tanikawa Hiromi (T)

Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China.

Jiaxing Tan (J)

Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China.

Sean Tanabe (S)

Department of Anesthesiology and Center for Consciousness Science, University of Michigan, Ann Arbor, MI, USA.

Stuart Fogel (S)

School of Psychology, University of Ottawa, Ottawa, Canada.

Anthony G Hudetz (AG)

Department of Anesthesiology and Center for Consciousness Science, University of Michigan, Ann Arbor, MI, USA.

Yihong Yang (Y)

Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Programs, National Institutes of Health, Baltimore, USA.

Emmanuel A Stamatakis (EA)

Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridge, UK.

Ying Mao (Y)

Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China. Electronic address: maoying@fudan.edu.cn.

Georg Northoff (G)

Institute of Mental Health Research, University of Ottawa, Ottawa, Ontario, Canada; Mental Health Centre, Zhejiang University School of Medicine, Hangzhou, China.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH